The origin of cultivated mangosteen (Garcinia mangostana L. var. mangostana): Critical assessments and an evolutionary‐ecological perspective

Abstract Mangosteen (Garcinia mangostana var. mangostana) is a popular tropical fruit, yet many aspects of its biology and evolutionary history are little known. Its origin remains contentious, although recent findings suggest G. mangostana L. var. malaccensis (Hook. f.) Nazre (synonym: G. malaccensis Hook. f.) as the sole progenitor. We review hypotheses on the origin of mangosteen and clarify points that have been affected by errors of fact and interpretation. The narrow focus and lack of detail in published results make their interpretation difficult. When possible, we support our interpretations with field observations and examination of herbarium specimens. We outline the main biological traits (e.g., dioecy, facultative apomixis, and polyploidy) of mangosteen and its wild relatives to infer traits that might have evolved during domestication of mangosteen. We find no clear indication that apomixis and polyploidy evolved during domestication. Polyploidy is known in the wild relatives, but apomixis has not yet been demonstrated. Also, we propose a testable new evolutionary‐ecological framework that we call “Forest‐Dusun Interface” to infer processes in the origin of mangosteen. Dusun (Malay) refers to subsistence orchards in this context. Lastly, we propose future studies to address identified knowledge gaps.

Despite a long history of cultivation, the domestication status of mangosteen, whether wild, domesticated, or semidomesticated (sensu C. Clement, 1999), is still being debated. Also, whether cultivated mangosteen has undergone substantial genetic adaptation to cultivated environments and consistent phenotypic changes under traditional cultivation management is still unknown. Under cultivation, has mangosteen evolved traits different from those of its wild ancestors, and if so, is it possible to retrace their evolutionary pathway? To answer these questions, we need to study the candidate wild progenitors, and to scrutinize the traits that may plausibly be expected to have been under selection during domestication.
We examine what little is known about these points. Some claims regarding the origin of mangosteen appear to be baseless (León, 1982;Zeven & de Wet, 1982), and theories of origin have been plagued with errors of fact and interpretation (Abdullah et al., 2012;Richards, 1990b). A thorough reappraisal is thus required. This review aims to provide a critical and in-depth evaluation of previous notions about the origin of mangosteen, to bring new insights on the domestication of this species, and to identify knowledge gaps.

| THE TA XONOMY AND DIS TRIBUTION OF GARCINIA S EC T. GARCINIA
The pantropical genus Garcinia comprises about 240 species (Stevens, 2001) of dioecious shrubs or trees (Sweeney, 2008) organized into 14 sections (Jones, 1980). The global distribution includes Central and South America, tropical Africa, Madagascar, the Mascarene islands, and throughout Southeast Asia to New Caledonia and northern Australia. Southeast Asia and Madagascar are the centers of species diversity (Sweeney, 2008). Garcinia is one of the most diverse tree genera in Asian tropical forests (Davies et al., 2005) but is poorly represented in the Americas (Stevens, 2007). The most recent global monograph for the genus is by Engler (1893Engler ( , 1925. Many species have been added and the concepts of taxonomic sections remodeled over time. Garcinia mangostana belongs to Garcinia sect. Garcinia. Recently, Nazre et al. (2018) published a taxonomic revision of this section and recognized 13 species. Taxonomic concepts of this revision are followed here. Because we cite synonyms of accepted names (and the use of synonyms is duly noted) where necessary to facilitate the coherence of discussions, it is crucial for us to list the accepted names and their synonyms in Table 1. In order to provide an idea of the phylogenetic position of G. mangostana in sect. Garcinia, we present a schematic phylogenetic tree ( Figure 1) adapted from Nazre's (2006) thesis. The closely related taxa repeatedly discussed in our study are illustrated with images.
The geographical distribution of sect. Garcinia spans across eastern India, Bangladesh, Indochina, and throughout Malesia. We tabulated the geographical distributions of all species of the section in Table 1. Geographical distributions and species richness of different areas within the region are shown in Figure 2.
An important outcome of the revision by Nazre et al. (2018) that is especially pertinent to the understanding of the origin of cultivated mangosteen was their recognition of three varieties of G. mangostana. Cultivated mangosteen is recognized as G. mangostana var. mangostana, G. malaccensis was synonymized as G. mangostana var. malaccensis, and a new variety, G. mangostana L. var. borneensis Nazre, was described. Comparisons of these varieties are summarized in Table 2. Notably, texture of the persistent stigma surface is identified as a diagnostic character  differentiating var. mangostana (smooth) from var. malaccensis (corrugated).
It is crucial to point out that distributions of G. mangostana var. malaccensis and G. penangiana Pierre, which have often been confused (see below), overlap in Sumatra (Hambali & Natawijaya, 2016), the Malay Peninsula, and Borneo, and sympatric populations of the two exist. Garcinia venulosa (Blanco) Choisy was thought to be confined to Luzon Island, Philippines, but our examination of herbarium specimens showed that this species is also found on other islands of this country, namely Mindoro, Samar, and Mindanao. The wild relatives of mangosteen, namely G. mangostana var. malaccensis and var. borneensis, are confined to everwet rainforests in Sumatra, Malay Peninsula, and Borneo (Hambali & Natawijaya, 2016;Nazre et al., 2018). Field observations (T.L. Yao) on the wild populations of var. borneensis showed that trees were generally found along ephemeral streams in low-lying flat land. Cultivated mangosteen also does best in environments with little water stress. Irrigation may be necessary during dry seasons (Osman & Milan, 2006).
The taxonomy of Garcinia is difficult (Sosef & Dauby, 2012), fraught with synonymies, and frequent misidentification of specimens. In this large genus, in which many species resemble one another in vegetative characters, identification to the species level is difficult when no reproductive organs are available. Garcinia penangiana is a species that has often been misidentified as G. malaccensis.
The confusion thereby introduced has contributed to clouding the interpretation of the origin of mangosteen (section 3.2). Examinations of the specimens deposited in regional herbaria revealed that many specimens of G. penangiana were systematically misidentified as G. malaccensis by various collectors. Other species are also concerned by such confusion. "Dr Kostermans has for some years now been labelling as G. celebica L. all specimens of this species-group [G. penangiana and other morphologically similar species] in the herbaria he has visited" (Kochummen & Whitmore, 1973 (Kochummen & Whitmore, 1973;Nazre et al., 2018;Ridley, 1922;, and G. malaccensis was regarded as the most late 1960s. These materials enabled him to expand and circumscribe the species concept of G. malaccensis. Idris and Rukayah (1987) described the male flower of mangosteen as having numerous stamens "surrounding a pistillode in a fourangled mass." They also compared the morphology of male flowers of G. mangostana with that of G. malaccensis and G. hombroniana.
However, Hambali and Natawijaya (2016) mentioned that the mangosteen male flowers described by Idris and Rukayah (1987)  The studies mentioned above defined the morphological characters of G. mangostana var. mangostana and the wild relatives. These findings enable us to identify the possible ancestral candidates of the cultivated mangosteen based on their morphological similarity.

| DOME S TI C ATI ON OF G . MANGOS TANA
Cultivated mangosteen, like many trees in cultivation, was most probably domesticated incipiently, making the definition of cultivated, wild, or feral very challenging (Clement, 1999). The status of mangosteen, whether wild or cultivated, has long been debated.
Views were contradictory in the early floristic accounts: "native and cultivated" (Anderson, 1874); "wild and cultivated" (King, 1890); and "cultivated… not known in the wild state" (Ridley, 1922) were descriptions of the states of cultivation. Corner (1952) opined that wild mangosteen populations were found in the then-virgin forests in Kemaman ( Figure 2) in Peninsular Malaysia, most likely vouchered as Corner s.n., 12 November 1935, Bukit Kajang Hillside, Kemaman, Terengganu, Peninsular Malaysia, barcode: SING0219178, which was later attributed to G. malaccensis  but to Corner's disagreement (Corner, 1997). Ashton (1988) mentioned that G. mangostana occurs in the wild on the east coast of Peninsular Malaysia and in Borneo. According to F. Slik (pers. comm.), "wild" mangosteen morphologically similar to cultivated mangosteen and with similar-tasting fruits was F I G U R E 1 (a). Schematic phylogenetic tree adapted from Figure 5.3 in Nazre (2006) depicting the affinity between the taxa discussed in the text. Names in box denotes taxa with multiple accessions. (b). Photographs of live plants and herbarium specimens of selected taxa.  borneensis is locally common in the lowland forests on the east coast of Sabah, Malaysian Borneo.
Fruit trees, especially durian (Durio zibethinus L.) and mangosteen, are planted by the Temuan communities in the logged-over timber production forest reserves in Peninsular Malaysia (T.L. Yao, pers. obs.). In the time before commercial logging, Temuan communities planted fruit trees in their old swiddens (Gianno & Bayr, 2009). (1893) Sulistiono, 2015). There is no information about whether the fruits were collected from forests or produced in orchards or home gardens. Notably, mangosteen was unequivocally transliterated as măng-jí-shì (莽吉柿) in Gong (2019) and Ma (2019) from manggis, a local name used consistently in coastal Borneo, Java, F I G U R E 2 Geographical distribution of taxa of Garcinia sect. Garcinia. Bioregions appear in bold typeface. Sundaland includes Sumatra, Malay Peninsula, Java and Borneo. The numbers denote total numbers of species and varieties represented in each region; numbers in parentheses indicate the total number of taxa endemic to the region. Garcinia mangostana var. mangostana is not included in these tallies. Points in red denote localities mentioned in the text. the west coast of the Malay Peninsula, and Sumatra throughout these few centuries. These regions correspond to the geographical extent of the core territories of the Majapahit Empire (1293-c.

CE).
An annotated glossary "Hobson-Jobson" (Yule & Burnell, 1886) detailed the origin of the name "mangosteen" and provided leads to a handful of early records about mangosteen documented in Western literature. de Orta et al. (1913Orta et al. ( [originally published in 1563) mentioned mangosteen and durian from Malacca in 1560's Portuguese Goa (de Orta et al., 1913) and implied that mangosteen was planted in Goa but had not yet yielded fruit at the time. The success of introduction, even if on a small scale and only for a short time, is shown by the mention of mangosteen in 1580's Portuguese India (van Linschoten et al., 1885). Followed by the burgeoning interest of early botanists in documenting exotic plant resources, especially those of economic value, accounts of mangosteen were presented in brief descriptions (Bauhin et al., 1650;Clusius, 1605;de Bondt, 1658) and listings (Bauhin, 1623). Mangosteen was deemed native to Malacca (Cardim, 1645), now a state in Peninsular Malaysia, and it was recorded as "growing within the bush by the highway in Java" Until the 1690s, mangosteen was thus considered to have originated from the Malay Peninsula, Sumatra and Java, where the major ports of sea trade routes were located. At this juncture, mangosteen was also documented in Herbarium Amboinense (Rumphius, 2011 [originally published in 1741]), a catalogue of the plants of Ambon ( Figure 2). In the text, mangosteen was considered foreign to Ambon but as being found in other Maluku islands (Figure 2), while Malacca, Sumatra, and western Java were stated to be the natural geographical range. Rumphius reported "Only one or two trees that bear fruits reasonably well" in Banda but stated that the trees "do much better in Ternate and Gilolo" (now Halmahera) owing to differences in soil properties. He made reference to Garcin's "de act. Paris. p. 431, Tab. 1", which is most likely the original publication that was translated into the English version in Garcin (1733)  Cultivated mangosteen is locally known as manggis; another cultivar is called mesta ( Table 2). The names manggis and mesta (or masta) do TA B L E 2 Comparison of the varieties of Garcinia mangostana (adapted from Nazre et al. (2018)). Based on written historical records, inference from linguistic evidence and field observations, we speculate that mangosteen originated in the everwet zones of Southeast Asia, including Sumatra, Malay Peninsula, and Borneo, but excluding islands with a relatively pronounced dry season such as Java and Maluku.

| What is the wild ancestor of G. mangostana var. mangostana?
In this section, we examine the taxa that have been proposed as the wild progenitors of mangosteen and critically examine the theories of its origin. Various hypotheses regarding the origin of mangosteen have been proposed (Table 3). Shaharudin et al. (2022) summarized and discussed these hypotheses but did not provide in-depth interpretation. We especially discuss these hypotheses in light of findings from molecular biology accumulated over the past few decades.
The proposed close affinity between G. malaccensis and G. mangostana (Corner, 1997;King, 1890;Kochummen & Whitmore, 1973;Nazre, 2006;Nazre et al., 2018; has been repeatedly supported in molecular-biological studies using various markers, that is, ITS (Nazre, 2014;Yapwattanaphun et al., 2004), AFLP (Sobir et al., 2009), RAPD (Sinaga et al., 2007), and ISSR (   opinion, based on morphological affinity, especially in vegetative characters, that G. hombroniana is one of the "close allies" of mangosteen. Another twist cropped up when Nazre (2014) pointed out that the cytological information for G. malaccensis alluded to in Richards (1990b) was actually based on a misidentification of G. penangiana sampled from Pasoh Forest Reserve (F.R.) (Figure 2), Peninsular Malaysia. Richards (1990b) cited Ha (1978), repeating that author's erroneous identification. As mentioned in Section 2, many specimens of G. penangiana have been misidentified as G. malaccensis, causing confusion. Unfortunately, we could not locate the voucher specimen no. 85 cited by Ha (1978) among the herbarium specimens we examined, but confirmed that other specimens collected by Ha in the same site in the same period were all G. penangiana. Dysploidy, or varying chromosome number counts, in mangosteen (Table 4) hampered emergence of a convincing interpretation of hybridization history based on chromosome counts.

Hypotheses References
*Originated from G. sylvestris or silvestris (a spelling variant) León, 1982;Zeven & de Wet, 1982 Hybrid of G. hombroniana and G. malaccensis Richards, 1990b Hybrid of G. opaca and G. malaccensis Abdullah et al., 2012 Hybrid of different varieties of G. malaccensis Nazre, 2014 Superior selections from female trees of G. malaccensis Incongruences between nrDNA and cpDNA phylogenetic trees can be related to hybridization events involving cytoplasmic captures but can also be explained by patterns of incomplete lineage sorting.
In addition to sample misidentification and misinterpretation of the findings, this study suffered from very small sample size. Yapwattanaphun et al. (2004) were first to demonstrate the phylogenetic relationships between mangosteen and 16 wild species using ITS sequences. Both unordered parsimony and neighborjoining analyses pointed to G. malaccensis as the closest relative of mangosteen. In more recent studies (Hambali & Natawijaya, 2016;Nazre, 2014), G. malaccensis is proposed as the sole progenitor of mangosteen.

| Mangosteen derived solely from G. malaccensis
Nazre (2014)   Wild mangosteen (2 n = 4x = 96). The chromosome counts of the latter concurred with the findings of Chennaveeraiah and Razdan (1975) and Tixier (1960). The study also revealed the occurrence of triploid forms (2 n = 3x = 72) in the wildlings grown in the garden, and the authors were able to produce the triploid form by artificial pollination of G. mangostana with G. malaccensis pollen in cross-breeding trials.
The  Harlan (1992) termed "diffuse origin". Mangosteen might have originated and diffused from its geographic origin(s) well before any written record existed.
Pierre (1882)  Descriptions of the practice of culling male trees by Chevalier (1919), which were later cited in Burkill (1966), are therefore dubious. To the best of our knowledge, no report of a practice of culling of male trees has appeared in other literature, nor is this practice known from any commercial orchard. However, the culling reported by Chevalier (1919) might have been a practice to eradicate those female trees that took a longer time to become productive.

Male organs on mangosteen flowers observed by
Chevalier (1919)  Very few data exist on sex ratio in populations of wild Garcinia spp.
During a flowering event, a field census of G. penangiana (misidentified as G. malaccensis) in Pasoh F.R. conducted by Thomas (1997) enumerated 31 staminate and 48 pistillate individuals. Male trees have been reported to be extremely rare in G. parvifolia (Miq.) Miq.

| Apomixis
Agamospermy may be frequent in Garcinia (Sweeney, 2008), and somatic embryogenesis has been demonstrated in cultivated mangosteen (Lim, 1984;Sprecher, 1919aSprecher, , 1919b. Asexual seeds are formed by an adventive embryo originating from a somatic cell in the epithelium of the inner integument layer of the ovary (Sprecher, 1919a(Sprecher, , 1919b. According to Horn (1940) and Lim (1984), mangosteen does not produce viable pollen. However, Horn's observations were based on shriveled flowers from two trees in an experimental station and may not constitute robust evidence. Lim (1984) conducted a bagging experiment to test whether pollen is required for seed production in mangosteen. On 50 bagged flowers, staminodes were left intact. On another 50 flowers, staminodes were removed prior to bagging. She found that flowers in both treatments set fruit, showing that fruit set did not require the presence of pollen. Fruit set in flowers from which staminodes had been removed (20%) was lower than in intact flowers (53%), owing probably to damage inevitably caused by manipulation during removal of staminodes. Unfortunately, there is no empirical genetic evidence for apomictic reproduction, e.g., highly similar or even identical multi-locus microsatellite genotypes between a mother tree and its progeny.
Hambali and Natawijaya (2016)  Roxb. and G. treubii Pierre (Treub, 1911). "Embryonic buds" formed on the inner integument were also observed in G. parvifolia and G. scortechinii King but do not develop into adventive embryos. In G. parvifolia, the unfertilized egg cell develops into an embryo (Ha et al., 1988

| Polyploidy
The postulated earliest event of evolution of polyploidy in Garcinia traces back to 86.3 MYA (Landis et al., 2018) and the dating of the whole-genome duplication event was inferred from analyses of the 1000 Plants (1KP) transcriptome data. Carman (1997) suggested that the base number of chromosomes is eight for Garcinia. The chromosomes of Garcinia are small and difficult to count Richards, 1990b). A number of Garcinia species variably display diploidy, dysploidy and polyploidy (  (Tixier, 1960) and 96 (Chennaveeraiah & Razdan, 1975), indicating possible diploidy and tetraploidy in the species. Chromosome number of G. mangostana var. malaccensis was first published only recently (Hambali & Natawijaya, 2016); diploidy and natural triploidy were observed. Polyploidy thus exists within species of sect. Garcinia and is not exclusive to mangosteen. The variation in chromosome number is notably greater in mangosteen than in related taxa, but this might be due to inadequate study of the wild taxa.
Polyploidy is well-documented in mangosteen (Hambali & Natawijaya, 2016;Midin et al., 2018). Matra et al. (2016)  and that polyploid species with a single rDNA locus can also be found (Garcia et al., 2017). Thus, the number of FISH signals does not allow inference of ploidy level.
Polyploidy in mangosteen is readily maintained by apomictic reproduction, which avoids potential difficulties in chromosome pairing during meiosis. However, whether apomixis is developmentally linked to autopolyploidy, as suggested for other plants (Grimanelli et al., 2001), or is instead an independently evolved phenomenon, remains unknown. We do not have enough information about the development of polyploidy in mangosteen or its wild relatives to assign them to any of the models presented by Hojsgaard and Hörandl (2019).
Differences in ploidy level within a species might be reflected in phenotypic variations (He et al., 2018;Ramsey & Ramsey, 2014).
borneensis is unknown. Due to ploidy variation and the presence of aneuploids , demarcating these entities using morphological characters remains a conundrum.

| Genetic variation
Progeny produced by apomixis are in theory genetically identical to the maternal plant (Hand & Koltunow, 2014). Apomixis in mangosteen led to the supposition that only limited genetic variation would be found within mangosteen populations (Horn, 1940), provided that all domesticates derived from a single original clone.
However, genetic variation was detected by various markers in mangosteens grown in Australia (Ramage et al., 2004;Sandø et al., 2005) and Indonesia ( It is essential to identify the sources of the observed variation.
Genetic variation in mangosteen might arise from three sources: (i) multiple selections of wild progenitors originating from independent events of sexual reproduction; (ii) heritable somatic mutation; and (iii) facultative apomixis that allows gene flow from wild populations. Sandø et al. (2005) and Nazre (2014)  Are somaclonal mutations the major source of variation in mangosteen, as Richards (1996) concluded for Taraxacum L.? Apomixis and other forms of asexual propagation are expected to lead to increased heterozygosity, because as somatic mutations are incorporated and transmitted, it is very unlikely that the same mutation will occur at the same locus on both chromosomes (Balloux et al., 2003). Variation at neutral loci may be notable in mangosteen, because this type of variation increases during somaclonal evolution. Microsatellite markers often evolve by stepwise mutations, so that if allele size diversity is small in relation to allele number diversity, this indicates recent differentiation (Hardy et al., 2003;Léotard et al., 2009), consistent with diversification via somaclonal mutation. Findings by Samsir et al. (2016) demonstrated that Simple Sequence Repeats (SSRs) alleles of mangosteen show little size variation, suggesting that they diversified via somaclonal mutations.
However, considering the level of genetic variation observed by Matra et al. (2016) in Javanese G. mangostana var. mangostana, it is unlikely that somaclonal mutations were the sole source of variation. Hambali and Natawijaya (2016) demonstrated that cross-pollination between mangosteen and wild G. mangostana var. malaccensis is possible. In this context, gene flow would be unidirectional from wild var.
malaccensis to cultivated mangosteen, with variation contributed only by pollen donors. Sexuality generally exists in perennial apomictic plants (Richards, 2003), and events of sexual reproduction in a generally apomictic line, although infrequent, can have a disproportionately large effect on genetic variability (Halkett et al., 2005).
Based on both empirical findings and theoretical arguments, the expectation that genetic variation is absent in mangosteen owing to its apomictic reproduction should be abandoned. However, the pattern of genetic variation in apomictic species is different from that in sexually propagated species.

| HYP OTHE S IS: DOME S TIC ATION AT THE FORE S T-DUSUN INTERFACE
Mangosteen is attractive to humans owing to its tasty fleshy fruits. As for other fleshy-fruited trees, its cultivation and eventual domestication may be seen as a process of humans taking over the function of seed dispersal from other frugivorous mammals.
Garcinia. The fruits are available on the trees for about four weeks and remain fresh for at least four weeks after falling to the ground. Individuals in both the wild and the cultivated compartments may have varied in ploidy levels in the forest-dusun interface. In this scenario, apomixis and polyploidy did not arise under domestication but were already traits of the plants selected for cultivation. Thomas (1997) suggested that apomixis could be advantageous for forest trees that typically occur at low population density.
How can we assess the plausibility of these two hypotheses? If G. In fact, fruits of cultivated mangosteen are larger than those of any other taxon in the section, including G. mangostana var. malaccensis , but it is currently impossible to determine whether this difference is genetically based or represents phenotypic plasticity in response to more favorable conditions in cultivated environments. Mangosteen has been available in markets for at least 600 years, probably even earlier at seaports of the regional maritime kingdoms, where exchanges of forest products were common. Early planting stocks might have been acquired from different sources throughout Sumatra, the Malay Peninsula and Borneo at different times over a long period and gradually diffused to the entire Malay Archipelago.
The current practice of growing mangosteen in commercial orchards isolated from natural populations reduced or halted gene flow between mangosteen and wild relatives. In commercial orchards where mangosteen reproduces exclusively apomictically, genetic variations between mother tree and progeny, if detected, may be principally due to the integration of somatic mutations.

CO N FLI C T O F I NTE R E S T S TATE M E NT
We declare no potential competing interest in our study and published findings.

DATA AVA I L A B I L I T Y S TAT E M E N T
No new data were created or analyzed in this review; data sharing is not applicable to this article.